A behavioural and ERP investigation of 3-month-olds’ face preferences

Abstract

Recent behavioural work suggests that newborns’ face preferences are derived from a general, non-specific attentional bias toward patterns with more features in the upper versus lower half. In the current study, we predicted that selectivity for the specific geometry of the face may emerge during the first 3 months of life as a product of perceptual narrowing, leading to the construction of the first broadly defined face category segregating faces from other visual objects which may share with faces one or more visual properties. This was investigated behaviourally, using a standard preferential looking paradigm, and electrophysiologically, using high-density ERPs. Behavioural results indicated that, at 3 months, the top-heavy property is no longer a crucial factor in determining face preferences. ERP results showed evidence of differentiation between the two stimuli only for the N700. No differentiation was found for earlier components that are thought to reflect the adult-like structural encoding stage of face processing in infants (N290 and P400). Together, ERP and behavioural results suggest that, by 3 months, the perceptual narrowing process has led to a behavioural response specific to the geometry of the human face, but that this response is not purely perceptual in nature. Rather, it seems related to the acquired salience of this stimulus category, which may reflect the high degree of familiarity and/or the social value faces have gained over the infants’ first 3 months of life.

Introduction

It has been reported in a number of behavioural studies that newborns’ visual attention is spontaneously and preferentially attracted toward face-like configurations. Specifically, it has been shown that when newborns are presented with upright and upside-down schematic face-like configurations (Johnson & Morton, 1991; Mondloch, Le Grand, & Maurer, 2003; Valenza, Simion, Macchi Cassia, & Umiltà, 1996) or real face images (Macchi Cassia, Turati, & Simion, 2004) that are matched for level of complexity, amount of energy, or both, they prefer those stimuli that display the upright structure of the face. These findings have been taken as evidence that, from birth, infants selectively respond to the geometry of the face, as defined by the correct relative location of the internal features for the eyes and the mouth (three dark blobs arranged in a triangular-shaped configuration with one vertex pointing down). Moreover, the newborns’ face preference phenomenon has been taken as one of the strongest pieces of evidence supporting the existence at birth of a biologically determined, experience-independent neural mechanism dedicated to face processing (Farah, 2000; Farah, Rabinowitz, Quinn, & Liu, 2000; Johnson & de Haan, 2001; Johnson & Morton, 1991). Based on a well-known case study demonstrating a lack of plasticity in the development of face recognition abilities, Farah et al. (2000) claimed that the anatomical cortical localization of face recognition is explicitly specified in the human genome. Alternatively, the developmental model of face processing proposed by Johnson and Morton (1991) (see also Johnson & de Haan, 2001) explains newborns’ face preferences as a result of the existence at birth of a specific face-detecting mechanism located subcortically rather than cortically. During the first 2–3 months of life, this subcortical mechanism (i.e., Conspec) would act as a guide, biasing visual input to the developing cortex and thus favouring the emergence of cortical circuitry specialized for face processing.

Regardless of whether the neural localization of face processing originates cortically or subcortically, both the aforementioned claims assume that a highly specific starting point is necessary to initiate development in the face domain. More recent behavioural work with newborns has questioned this assumption, suggesting that face processing at birth is mediated by general, rather than domain-specific perceptual processes. This work showed that newborns’ face preferences derive from a number of more general attentional biases that cause certain structural properties of a visual stimulus to be preferred, rather than from a content-determined bias for the unique geometry of the face (Simion, Macchi Cassia, Turati, & Valenza, 2003). In fact, much evidence is now available supporting the contention that the visual structural properties embedded in the face are capable of producing a preferential response also when they are embedded in non-face stimuli (Macchi Cassia, Valenza, Pividori, & Simion, 2002; Simion, Valenza, Macchi Cassia, Turati, & Umiltà, 2002). Specifically, one of these structural properties (i.e., up-down asymmetry) relates to the up-down asymmetrical distribution of the inner facial features along the horizontal plane (i.e., faces typically display two features – the eyes – in the upper part and one feature – the mouth – in the lower part) (Macchi Cassia, Turati, & Simion, 2004; Simion et al., 2002, Turati et al., 2002).

The results of a recent study, in which natural and scrambled real face images were used as stimuli, showed that newborns attend equally long to a face as to a non-face “top-heavy” stimulus that shares with faces the same up-down asymmetrical distribution of the elements (Macchi Cassia et al., 2004). In this study, newborns showed a preference for an upright over an upside-down face (Macchi Cassia et al., 2004, Experiment 1), and for a non-face top-heavy pattern over a non-face-like bottom-heavy pattern (Macchi Cassia et al., 2004, Experiment 2). Importantly, when newborns were presented with a face and a non-face-like top-heavy pattern that were equated for the number of features appearing in the upper and lower halves (i.e., two features and one, respectively), they did not manifest any spontaneous preference (Macchi Cassia et al., 2004, Experiment 3; see Table 1). This demonstration that the face-like arrangement of the inner features displayed by the natural face did not affect newborns’ visual behaviour was taken by the authors as evidence that what is classically interpreted as a specific inborn preferential response to faces is in fact the result of a more general preference for any class of top-heavy visual stimuli displaying more patterning in the upper portion. Indeed, stimuli within this category include, but are not limited to faces. The authors suggested that this attentional proclivity toward the top-heavy stimulus category likely derives from endogenous constraints of the newborns’ visual system (i.e., an upper versus lower visual field advantage in visual sensitivity similar to that observed in adults, Skrandies, 1987), which renders top-heavy patterns more easily detectable for newborns than other stimuli.

The evidence provided by these studies with newborns seems to fit well with the perceptual narrowing account of the development of face processing proposed by Nelson, 2001, Nelson, 2003, according to which the ability to perceive faces narrows with development based on experiential input. This model suggests that the face specificity assumed in the adult neural and perceptual system arises from a general-purpose perceptual system that, during development, becomes progressively tuned to upright human faces, due to the extensive experience with this stimulus category reliably provided by the species-typical environment. The narrowing of the perceptual window would thus produce a more precisely defined face category comprised of the type of faces seen most often in the environment, for which more efficient strategies of perceptual processing may be utilized. The neurophysiological counterpart of this process of perceptual narrowing would be an increase in the selectivity and localization of the cortical circuits involved in face processing (Johnson, 2000). Over time, these circuits would pass from being activated by a broader range of stimuli to responding to only certain kinds of stimuli, thus giving rise to a more localized and specialized neural response. Note that this recently proposed model of the development of face processing differs from that previously proposed by Johnson and Morton (1991) (see also, Johnson & de Haan, 2001) in that it assumes that general, rather than specific initial input, is sufficient to set the stage for the development of the face recognition system into its adult-like, specialized form. Some of the strongest evidences supporting the idea of a perceptual narrowing process with respect to face perception comes from behavioural and event-related potential (ERP) studies that compared processing of human faces to that of non-human primate faces in infants over the first year of life, and adults, testing what is known as the “other-species effect”. Behavioural studies showed that although 6-month-olds, 9-month-olds and adults are all equally capable of discriminating two human faces, 6-month-olds are superior to older infants and adults in discriminating monkey faces (Pascalis, de Haan, & Nelson, 2002). In line with these results are findings from ERP studies showing increasing selectivity, between 6 and 12 months, to upright human (versus monkey) faces at the two components that have been proposed as possible “developmental precursors of the adult N170” (de Haan, Johnson, & Halit, 2003), namely the N290 and P400 (de Haan, Pascalis, & Johnson, 2002; Halit, de Haan, & Johnson, 2003). The N170 is a well-documented, face-specific component that is used as an electrophysiological marker for specialized mechanisms for face processing in adults (after Bentin, Allison, Puce, Perez, & McCarthy, 1996). Evidence concerning the development of the N290 and P400 suggests that, between 6 and 12 months, the face processing system has become more finely tuned to upright human faces.

In addition to these findings, some earlier behavioural studies examining infants’ preference for face-like stimuli offer indirect evidence supporting the idea that, with increasing experience with faces, infants’ preferential responses to faces become tuned to more specific characteristics of this stimulus category. For example, it has been reported that the preference that newborns show for an upright highly schematic face-like configuration (i.e., three square blobs arranged as facial features) over its inverted counterpart disappears by 6 weeks (Johnson, Dziurawiec, Ellis, & Morton, 1991; Mondloch et al., 1999). Moreover, 12- but not 6-week-old infants show a preference for a positive contrast schematic face over a negative contrast version of the same face (Dannemiller & Stephens, 1988; Mondloch et al., 1999). Together, these results suggest that, between birth and 12 weeks of age, infants’ behavioural responses start to depend more on the extent to which various characteristics of the stimuli resemble those included in real faces. Relevant to the aim of the present study, this evidence could be interpreted as a demonstration that, by 12 weeks, up-down asymmetry by itself is no longer sufficient to drive infants’ face preferences, but rather other characteristics of the face stimuli have begun to play a more crucial role.

The goal of the current study was to provide direct support for the hypothesis that a process of perceptual narrowing, analogous to that reported to take place for faces of our own species between 6 and 9 months of life, may take place even earlier in development, leading to the construction of the first broadly defined face category segregating faces from other visual objects which may share with faces one or more visual properties. Specifically, we hypothesize that perceptual and neural selectivity for the specific geometry of the face may emerge during the first 3 months of life arising from the non-specific attentional bias toward top-heavy patterns that is present at birth (Macchi Cassia et al., 2004). Because this attentional bias causes faces to be a frequent input to the developing face processing system, we could expect that, by 3 months of age, faces might have emerged as a separated class of stimuli from other geometrically similar stimuli (i.e., top-heavy patterns). At the behavioural level, this perceptual narrowing process would result in increased attention triggering values of faces as compared to other non-face top-heavy visual stimuli, with respect to what has been found in newborns. At the neural level, we would expect to observe a difference in the neural response to the two different object categories of faces and other non-face top-heavy stimuli.

Both these hypotheses were investigated in the current study by using a between-subjects design, in which behavioural and ERP data were obtained from two different groups of 3-month-old infants. To determine whether, at 3 months of age, infants preferentially orient their visual attention to faces as compared to other non-face top-heavy patterns, we used the same behavioural paradigm – preferential looking – and the same set of natural and scrambled top-heavy and bottom-heavy images derived from real faces as those used in the newborn study by Macchi Cassia et al. (2004) (see Table 1). In the ERP study, we attempted to gain converging evidence for the differential processing of faces and non-face top-heavy stimuli in 3-month-olds by recording ERPs as infants viewed natural and scrambled top-heavy real face images.